Content uploaded by Philip David Round
Author content
All content in this area was uploaded by Philip David Round on Dec 14, 2018
Content may be subject to copyright.
661
Conservation Biology, Pages 661–671
Volume 17, No. 3, June 2003
Issues in International Conservation
Causes and Effects of Temporospatial Declines of
Gyps
Vultures in Asia
A Global Perspective of
Gyps
Vultures
There are eight species in the genus
Gyps
:
Gyps africanus
,
G. coprotheres,
and
G. rueppellii
in Africa;
G. benga-
lensis
,
G. indicus
,
G. tenuirostris
,
G. himalayensis
in Asia;
G. fulvus
in
Europe, Africa, and Asia. The ranges of
many of these species overlap, and
wintering
G. fulvus
overlap with sev-
eral resident species in Asia and Africa
(Fig. 1).
Gyps
species share a similar
feeding ecology, scavenging the soft
tissues of large mammals, usually un-
gulates. They tend to be colonial nest-
ers and communal feeders, feeding
alongside conspecifics and other
vulture species. Densities of
Gyps
vul-
tures can be high in areas with suit-
able breeding habitat and abundant
carrion. An extreme example is
G. ben-
galensis
, which often lives in close as-
sociation with humans. During the
1970s and early to mid-1980s, densi-
ties of 12 nests/km
2
were recorded at
Keoladeo National Park, Rajasthan, In-
dia (Prakash 1989), and there were
nearly 3 nests/km
2
in the city of Delhi
(Galushin 1971 ), where flocks of sev-
eral thousand birds were present at
carcass dumps. As recently as 1985,
G. bengalensis
was regarded as “pos-
sibly the most abundant large bird of
prey in the world” (Houston 1985 ).
Despite
Gyps
population declines
across Southeast Asia, until recently
only one species of Africa,
G. copro-
theres,
was considered globally
threatened (vulnerable; BirdLife In-
ternational 2000), largely because of
the indiscriminate use of poisons in
southern Africa (Mundy et al. 1992).
Following the recent population crash
in
Gyps
species across the Indian
subcontinent, three other species,
G. bengalensis, G. indicus,
and
G.
tenuirostris
, are now listed as criti-
cal ( BirdLife International 2000),
placing them among the most threat-
ened birds in the world.
Historical Declines and Likely
Causes in Southeast Asia
During the first half of the twentieth
century, two species of
Gyps
vulture
(
G. bengalensis
and
G. tenuirostris
)
were well distributed and often spe-
cifically noted as abundant in South-
east Asia (including adjacent Yun-
nan Province, China). By the end of
that century, both species were ex-
tinct across almost the entire area. A
small area of northeastern and north-
ern Cambodia holds relict popula-
tions of both species, with some ex-
tension into adjacent parts of Laos
and Vietnam. Elsewhere in these
countries, and in Malaysia, Thailand,
and Yunnan, the few recent records
probably indicate wandering birds.
The situation in Myanmar remains
unclear, but a major decline has also
occurred there, at least locally. Table 1
illustrates changes in populations of
G. bengalensis
over this period.
The breeding success of remain-
ing birds in Southeast Asia appears
to be low (Timmins & Ou Ratanak
2001). Uncontrolled hunting has led
to wholesale population collapses of
wild ungulates in this region (Sriko-
samatara & Suteethorn 1995; Duck-
worth et al
.
1999; Hilton-Taylor 2000)
that, together with changes in hus-
bandry of domestic stock (Cambo-
dian Wetland Team 2001), have re-
sulted in a huge reduction in the
carrion available for vultures. It
seems likely that food supplies are
no longer predictable enough to al-
low regular breeding. Persecution of
vultures when they are gorged on
carcasses and at nests may also have
played a role (Thewlis et al
.
1998).
Persecution may be at a level that
makes birds shy enough to be af-
fected by incidental disturbance (au-
thors’ unpublished data), and, given
the high human density across much
of the region, this factor should not
be underestimated. Habitat loss, ex-
cept insofar as it has contributed to
ungulate declines, can be discounted
as anything other than a local threat
(Thewlis et al
.
1998). The role of
agrochemicals remains unclear;
there is no persuasive indication that
they can explain region-wide losses
in Southeast Asia, although they
may have caused local declines (Cheke
1972).
Circumstantial evidence suggests
that infectious disease was not a
cause of this decline or today’s ex-
tremely low population density. The
decline affected not only
Gyps
vul-
tures but also all other scavenging
birds, such as the Red-headed Vulture
(
SarcoGyps calvus
), Greater Adjutant
(
Leptoptilos dubius
), Black Kite (
Mil-
vus migrans
), Brahminy Kite (
Hali-
astur indus
), and Large-billed Crow
(
Corvus macrorhynchos
). The status
of these species varies across the re-
gion, with perhaps the steepest de-
clines in Laos, where even the Large-
billed Crow is absent from large areas
(Lekagul & Round 1991; Thewlis et
Conservation Biology
Volume 17, No. 3, June 2003
662
Issues in International Conservation Pain et al.
al. 1998; Wells 1999; Duckworth et
al. 1999, 2002; Round 2000).
Although vulture declines have
been marked throughout Southeast
Asia, there is some patchiness to the
severity of the losses, again with
Laos having suffered some of the
steepest declines. This comparison
is instructive because the country re-
tains large tracts of habitat suitable
for these species, has a relatively
low human population density, and
is unlikely to have used environ-
ment-contaminating chemicals at
high levels across the ancestral vul-
ture range. Laos did, however, lose
most of its open-country wild ungu-
lates during the second half of the
twentieth century (through hunting),
and it probably experienced signifi-
cant changes in livestock husbandry
(Duckworth et al. 1999). Cambodia,
the core area for the relict
Gyps
pop-
ulations of Southeast Asia, differs
from the rest of Indochina. A rela-
tively large open-country landscape
has until recently remained sparsely
settled (because of the Khmer Rouge
and other security concerns), wild un-
gulate populations persist locally, and
the villages in and abutting this area
still practice extensive free-ranging
of domestic bovids during the dry
season (Timmins & Ou Ratanak 2001).
The remnant
Gyps
populations in ad-
jacent Laos and Vietnam are unlikely
to be viable under current condi-
tions without this Cambodian vulture
population.
Although data are too scant to be
certain of the reasons for the
Gyps
de-
clines in Southeast Asia, food shortage
appears to be the most credible gen-
eral explanation, although other fac-
tors including persecution and contam-
inants may have played a part locally.
Recent Declines across the
Indian Subcontinent
During the 1970s and 1980s, when
Gyps
vultures were absent or scarce
across most of Southeast Asia (Table
1),
G. bengalensis
, and to a lesser
degree
G. indicus,
remained ex-
tremely abundant in India, especially
around towns and cities. This abun-
dance resulted from the large num-
ber of cow carcasses available for
vultures in northern and central
states of India, where religious be-
liefs prohibit their slaughter (Grubh
et al. 1990). Cattle carcasses are left
in the open in rural areas and, along
with slaughterhouse offal, are taken
to carcass dumps outside the towns
and villages, where vultures con-
sume them. Numbers of vultures
around settlements were so high in
the 1980s that they were considered
a serious hazard to aircraft (Grubh et
al. 1990 ). During the 1980s and
1990s, numbers of
G. bengalensis
and
G. indicus
were monitored at
Keoladeo National Park ( KNP ), a
World Heritage Site in eastern Rajast-
han. Prakash (1999) recorded
95%
declines in numbers of these two
species in the park between the mid-
1980s and late 1990s.
G. bengalen-
F
igure 1. Breeding and wintering distribution of Gyps vultures in the old world (after Mundy et al. [1992] and
based on updated distribution information from Robson [2000]). The Southeast Asian range shown is historical.
Conservation Biology
Volume 17, No. 3, June 2003
Pain et al. Issues in International Conservation
663
Table 1. Population status and distribution of
Gyps bengalensis
in Asia in throughout the twentieth century.
Country
Pre-1950 population
and distribution
Post-1950 population
and distribution
Last record
and location
Reference
*
Southeast Asia
China no records, but survey of
Yunnan patchy
southwest only (Yunnan province );
scarce or rare
southern Yunnan, 1959 & 1960;
now considered extinct
Tso-hsin 1987;
Guangmei & Qishan 1998
Myanmar widespread and common,
including large numbers in
towns and suburbs
scarce in many areas by 1950s;
subsequent history poorly known
still localized small numbers (Chin
Hills & Kachin State); status poorly
known
Smythies 1953;
Robson et al. 1998
Thailand widespread resident
throughout country; fairly
common to locally
abundant
still fairly common in 1960s but rare by
1970s and almost extinct by 1980s
probably extinct as a breeding bird;
occasional reports of individuals
until winter 2000
Deignan 1945, 1963;
Round 1988; Wells 1999;
P.D.R., unpublished data
Malaysia fairly widespread resident,
still common in 1930s
by mid-twentieth century, almost
extinct, except adjacent to Thailand
few records, rare nonbreeding visitor
(Kampung Penyirang, June 1979)
Wells 1984, 1999
and references therein
Laos widespread and common to
abundant
1950s–1980s poorly known; by 1990s
restricted to far south
very small numbers in southern
provinces of Champasak & Attapu;
could become extinct
(2000 )
Thewlis et al
.
1998;
Duckworth et al. 1999
and references therein
Cambodia once relatively abundant in
suitable habitat
data patchy, but by late 1990s, when
survey work resumed, only a few
populations remained
centered on the northeast provinces
of Preah Vihear, Stung Treng,
Mondulkiri, and Ratanakiri
Timmins & Men Soriyun
1998; Goes 1999; BirdLife
International 2001;
Timmins & Ou Ratanak
2001; J.W.D., C.M.P.,
R.J.T., unpublished data
Vietnam
widespread, locally abundant
resident in central and
southern regions
widespread and commonest vulture in
south Vietnam until at least late 1960s
one adult in Dak Lak province, 1997–
1998; other nationwide surveys
found none
Delacour & Jabouille 1931;
Wildash 1968; Le Xuan
Canh et al
.
1997
Indian subcontinent
India widely distributed resident
throughout all but
southernmost tip;
common to abundant
widespread and abundant to very
abundant until the mid-late 1990s,
when population crashes were
reported throughout the country
still widespread but at comparatively
low densities; local extinctions have
wiped out many colonies
Rahmani 1998;
Prakash 1999;
Prakash et al
.
2003
Nepal widespread and common
throughout lowlands
widespread and common throughout
lowlands; local population declines
reported over last few decades (e.g.,
Chitwan)
still recorded throughout lowlands
but high mortality and population
declines have occurred since late
1990s
Scully 1879; Rand &
Fleming 1957; Inskipp &
Inskipp 1991
Bhutan no records
records from Bhutan date from 1991–
1999; uncommon to approximately 100
birds near Teesta valley in mid-1990s
birds seen in several places in early to
mid 1990s, but few birds reported
since 1998
Inskipp & Inskipp 1993;
BirdLife International 2001
and references therein
Bangladesh widely distributed and
common
widespread; still relatively common but
numbers lower than in 1980s and
early 1990s
locally common throughout the
country and a common resident
breeder in village areas
Husein & Sarkar 1971;
BirdLife International 2001
and references therein
Pakistan widespread and common
resident in suitable habitat
(e.g., Indus plain )
widely distributed in many areas and
may have expanded into new areas in
Sindh post 1960s; abundant in Indus
plain (Punjab, Sindh, Northwest
Frontier) by 1991
still widely distributed; large-scale
mortality in many areas over last 5
years (see text )
Roberts 1991–1992;
BirdLife International 2001
and references therein
*
Reference is given to a recent national status overview where available; these are indicated by “and references therein.” For countries lacking a recent status overview, key historical and re-
cent references are listed, with BirdLife International (2001) as a general regional source.
Conservation Biology
Volume 17, No. 3, June 2003
664
Issues in International Conservation Pain et al.
sis
used to nest at KNP, and num-
bers of nests declined from 250–350
in the mid-1980s to none by 2000
( Prakash 1999; Prakash et al. 2003 ).
Nesting success ( total number of
active nests producing young) de-
clined from 82% in 1985–1986 (
n
244 nests) to zero in 1997–1998 (
n
25) and subsequently. The declines
were associated with high adult and
juvenile mortality, and small num-
bers of birds were observed in a
weakened state perched in trees in
the park. In general, these birds re-
tained a characteristic slumped pos-
ture with drooping necks for several
weeks before dying. In 1985 and
1986,
1700
G. bengalensis
were re-
corded in KNP, and 14 birds (7 adult,
7 juvenile ) were found dead. In
1997–1998, when the population
numbered just a few hundred birds,
73 adults and 10 juveniles were
found dead. The population decline
and high mortality was unexplained.
The food supply had not altered over
the period of decline, and no other
avian genera were similarly affected.
The dramatic and unexplained de-
clines at KNP, along with unsubstanti-
ated reports of vulture declines from
across the country, prompted the Bom-
bay Natural History Society to conduct
wide-scale vulture surveys in 2000.
These were repeats of surveys con-
ducted in 1991–1993, which covered
states in north, west, and east India.
Minimum declines in numbers of
G.
bengalensis
and
G. indicus
of 96%
and 92%, respectively, were recorded
(Prakash et al. 2003). (
G. indicus
is
now considered to include two distinct
species, the Indian Vulture [
G. indi-
cus
] and the Slender-billed Vulture
[
G. tenuirostris
] [Rasmussen & Parry
2000]. We treated
G. indicus
as one
species because the two forms were
not differentiated during fieldwork.
However, most of the birds recorded
in west Bengal within the “east region”
were
G. tenuirostris
. Because declines
were similarly elevated in all areas,
G.
tenuirostris
and
G. indicus
have prob-
ably declined to a similar extent.)
The extent of declines did not differ
between protected and unprotected
areas, and although there was some
evidence for larger declines in the
north than in the west, declines of
G.
bengalensis
were
90% in all regions.
Also, apparently sick birds with droop-
ing necks were reported in all regions.
Preliminary results from repeated sur-
veys in 2002 indicate that, at least for
G. bengalensis
, declines have contin-
ued, resulting in many local extinc-
tions ( V.P., unpublished data).
High mortality and declines in
Gyps
vultures have recently oc-
curred in neighboring Nepal and Pa-
kistan. In Nepal, high adult mortality
was recorded in
G. bengalensis
dur-
ing the 2000–2001 breeding season at
Koshi Tappu Wildlife Reserve (east-
ern Nepal). Although the breeding
colony is relatively small (67 nests
found, of which 27 were active), 45
G. bengalensis
were found dead, 34
(75.5% ) of which were adults ( Vi-
rani et al. 2001). In Pakistan, during
the 2000–2001 breeding season, Gil-
bert et al. (2002 ) estimated minimum
annual mortality rates in the adult
breeding populations of
G. benga-
lensis
from two colonies to be 11.4%
and 18.6%. The authors acknowledge
that these are likely considerable un-
derestimates because they assume that
( 1 ) all dead birds were found (in
fact, only carcasses in the immediate
vicinity of nests not removed by
scavengers were found) and ( 2 ) only
dead adults were used to estimate
annual mortality in the breeding pop-
ulation ( whereas an unknown pro-
portion of the breeding population
had subadult plumage).
High mortality, especially of
adults, and low breeding success
caused the population declines in In-
dia, Pakistan, and Nepal.
Gyps
vul-
tures are generally long-lived; one
captive
Gyps fulvus
lived for 37
years (Newton 1979 ). They repro-
duce slowly, reaching maturity in 4–
6 years, and produce one egg during
breeding years ( Mendelssohn &
Leshem 1983; Simmons 1986; del
Hoyo et al. 1994). Adult survival is
high. Wild-born
G. fulvus
from a re-
introduced, increasing population in
France had mean adult survival rates
of 0.987
SE of 0.006 and juvenile
(
3 years old ) rates of 0.857
0.039 (Sarrazin et al. 1994).
Causes of Declines across the
Indian Subcontinent
In contrast to the relatively slow de-
clines of
Gyps
vultures in Southeast
Asia, Indian populations have declined
by
95% within the past decade, a
rate of decline unprecedented among
common raptors in its rapidity and
one that appears to be continuing.
There are several possible explana-
tions for the high mortality and re-
duced breeding success of
Gyps
vul-
tures in southern Asia, including
food shortage, persecution, contami-
nants, and infectious disease.
Food Shortage
Although there is convincing cir-
cumstantial evidence to implicate
food shortage in
Gyps
declines in
Southeast Asia, food availability has
remained high throughout the In-
dian subcontinent during the period
of decline. During vulture surveys in
India in 2000, Prakash et al. (2003)
recorded numbers of livestock car-
casses seen and their attendant scav-
engers. Of 262 carcasses seen, only
12 (
5% ) had vultures present;
most were attended by crows
Cor-
vus
spp. and feral dogs. Counts of
Gyps
vultures at three carcass
dumps that remained active be-
tween 1990 and 2000 showed de-
clines of 87–100% in numbers of vis-
iting vultures. In 1999, of 1920
completed questionnaire returns,
approximately 80% of respondents
indicated that dumping of carcasses
in the open remained the predomi-
nant form of disposal in their region
(Prakash et al. 2003). Although car-
casses remained common and avail-
able to vultures, there was some
indication that they were less abun-
dant than 10 years ago (76% of re-
spondents reported carcasses as
fairly or very common in 1990; 63%
in 2000).
Conservation Biology
Volume 17, No. 3, June 2003
Pain et al. Issues in International Conservation 665
Although few data exist, there is
some evidence that the Red-headed
Vultures, underwent a significant
(p 0.03 ) but less severe ( 48%)
population decline between 1991–
1993 and 2000 (Prakash et al. 2003).
It is conceivable that, in the absence
of the mortality factor that has
caused the Gyps population crash,
numbers of avian scavengers could
be declining slowly in India due to a
gradual reduction in available food.
Although monitoring data are scarce,
populations of other scavenging birds
show no obvious signs of decline,
and some scavengers, such as feral
dogs, are reported to be increasing
across India ( Cunningham et al.
2001). Finally, there has been no ev-
idence of starvation being a contrib-
uting factor to the death of vultures
necropsied from across India and Pa-
kistan (Gilbert et al. 2002; Prakash et
al. 2003). Consequently, food short-
age is an unlikely explanation for the
recent vulture population crash
across the Indian subcontinent.
Persecution
Persecution, particularly through de-
liberate or accidental poisoning, can
have a significant impact on raptor
populations, especially on commu-
nal feeders such as vultures. Poisoning
campaigns eliminated scavenging birds
and large eagles from the huge stock
farming area of Namibia in the
1980s. In the neighboring national
parks of Kalahari Gemsbok and Etosha,
however, these same species remained
abundant (Mundy et al. 1992 ). While
a significant threat in Africa, persecu-
tion is unlikely to have played a large
part in vulture declines across the In-
dian subcontinent. Vultures are gen-
erally valued within Indian society
for their role in environmental
health. They also have an important
cultural and religious significance.
The Parsee religion depends upon
vultures to remove their dead, and
the vulture saint, Jatayu, is an impor-
tant figure in Hindu religion. Some
poisoning almost certainly occurs,
but it is unlikely to have more than a
local impact and cannot explain
rapid nationwide declines of the
type experienced by Gyps spp. This
is because, as in Africa, such poison-
ing would likely affect other avian
scavengers, such as the Steppe Eagle
(Aquila nipalensis), and would re-
sult in regional differences in rates
of decline. However, there is no evi-
dence that this is happening.
Contaminants
Chemical poisoning by contami-
nants in widespread use, such as ag-
ricultural chemicals, could result in
massive mortality and reduced
breeding success in raptors at a na-
tional scale, as DDT did in many
countries (Ratcliffe 1967a, 1967b;
Newton et al. 1982, 1986 ). Large
amounts of pesticides are used in In-
dia, and use increased considerably
in India in the 1980s. Official statistics
indicate overall declines in pesticide
use through the 1990s (Directorate
of Economics and Statistics website
http://agricoop.nic.in/statistics/
consum1.htm), but this masks trends
in individual chemicals and chemical
groups. For a chemical to cause the
widespread vulture declines re-
corded, it would need to have been
either introduced de novo and ap-
plied across a huge geographical area
or used previously and applied in a
novel way that increased its availabil-
ity to vultures within the last 10–20
years. No pesticides have been iden-
tified that obviously meet these crite-
ria. Toxicological analyses have been
conducted on many dead vultures
from Pakistan, and tissues have been
tested for organochlorines, organo-
phosphates, carbamates, and heavy
metals. None of these substances
have been detected at levels consis-
tent with toxicity (Oaks et al. 2001).
This and the lack of regional patterns
in the declines and obvious effects in
any other genera of scavenging bird or
mammal suggest that contaminant poi-
soning alone is unlikely responsible for
the declines. Little wildlife monitoring
exists, however, and the role of con-
taminants cannot be discounted.
Infectious Disease
The rapidity and ubiquity of the vul-
ture declines in India suggest either
a simultaneous subcontinent-wide
exposure to a toxic contaminant or
a rapid spread of disease through the
Gyps vulture population. The occur-
rence of declines across interna-
tional borders, the patterns of mor-
tality, and the declines in breeding
and roosting colonies are more
indicative of the latter than the
former. Once birds exhibit the neck-
drooping condition, the illness,
which appears to be invariably fatal,
gradually spreads throughout the
colony over a period of several years
(Cunningham et al. in press; Prakash
et al. 2003 ). No affected colonies
have recovered from this mortality
factor, although further data are re-
quired to verify this. It is unknown
whether colony extinction is due
entirely to vulture mortality or
whether, once the population num-
ber or density falls below a certain
level, surviving (and possibly in-
fected and infectious) vultures desert
the site to join other colonies.
Postmortem analyses of G. benga-
lensis, G. indicus, and one G. hima-
layensis from India (Cunningham et
al. 2001, in press; Pain et al. 2002)
and G. bengalensis from Pakistan
(Oaks et al. 2001; Gilbert et al. 2002 )
identified renal and visceral gout (crys-
tallization of uric acid in the tissues)
in the majority of birds found dead,
and enteritis in a high proportion of
the birds from India (Cunningham
et al., 2001, in press). Few other gross
findings are consistently observed.
The presence of visceral gout in tis-
sues of dead birds from both coun-
tries supports the hypothesis that
the same mortality factor is responsi-
ble for all these deaths. Although re-
nal gout is often attributed to kidney
disease, in these cases the gout was
acute (i.e., occurring only a few hours
before death), suggesting that this con-
dition is a consequence of the pri-
mary disease and not the disease it-
self (Cunningham et al. 2001, in press).
Visceral gout and enteritis are non-
Conservation Biology
Volume 17, No. 3, June 2003
666 Issues in International Conservation Pain et al.
specific lesions and could result
from, for example, a contaminant in-
sult or an infectious disease process.
Histological analyses of tissues from
Indian birds, however, found higher
than expected proportions of vul-
tures with inflammation of blood
vessel walls and proliferation in the
brain of glial cells (inflammatory cells
specific to the central nervous system)
(Cunningham et al. in press). In the
absence of findings other than vascu-
litis, gliosis is generally associated
with viral infection.
The epidemiology of vulture mor-
tality, which includes pandemic de-
clines, apparent rapid spread to
other countries, and specificity to
the genus Gyps, is consistent with a
hypothesis of infectious disease. Post-
mortem findings and the lack of pos-
itive toxicological results similarly
support this hypothesis. Although
we cannot be certain that an infec-
tious disease is responsible until a
causal agent has been identified, this
is currently the most tenable hypoth-
esis, so it is important to consider
the implications of this explanation.
Potential Spread outside Asia
There are eight species in the genus
Gyps distributed across Asia, the Mid-
dle East, Europe, and Africa (Fig. 1).
The risk of disease spread from the In-
dian subcontinent depends on many
factors: whether the disease will cross
species barriers, the rate and method
of transmission, the time course be-
tween infection and death, the period
of infectiousness, the degree of isola-
tion of individual species, and others.
Three Gyps species (G. bengalensis,
G. indicus, G. tenuirostris ) have
been affected by the same mortality
factor in India, Pakistan, and Nepal,
although a fourth (G. himalayensis)
may also be affected (Cunningham
et al. in press). All eight Gyps species
may therefore be susceptible. The rate
of the declines across India and ap-
parent spread into Pakistan and Nepal
suggest a highly infectious disease.
Transmission is probably facilitated
by the species’ behavior: they breed,
roost, and feed communally and travel
great distances (Houston 1974, 1983 ).
To evaluate potential spread and its
effects, let us assume in a worse-case
yet realistic scenario that infectious
disease is the sole cause of the de-
clines and that it can affect all mem-
bers of the Gyps genus with fatal
consequences.
No Gyps species is completely
geographically isolated from its con-
generics (Fig. 1 ). All Gyps species
forage widely (Houston 1974, 1983 ),
and juveniles may disperse more
widely or be more nomadic than
adults. G. fulvus breeding in Turkey
are migratory, and in many regions
immature individuals undertake dis-
tinct north-south migrations (del Hoyo
et al. 1994; Ferguson Lees & Christie
2000). Birds from Western Europe
cross the straights of Gibraltar to
North Africa ( e.g., 2160 birds re-
corded in autumn 1993; Griesinger
1996). Eastern populations from Asia
and the Middle East migrate to North
and East Africa, although migration
routes are unknown. In recent years,
unusually large numbers of juvenile
G. fulvus of unknown origin have
been overwintering in western India
(e.g., approximately 850 were seen at
a single carcass dump in western
Rajasthan in January 2002; Prakash et
al. 2003), presumably because of the
increased availability of food. It is not
yet clear, however, whether they are
susceptible to the mortality factor af-
fecting other Gyps vultures. It is possi-
ble that birds infected in India will not
show evidence of disease while in In-
dia because the incubation period is
unknown. Also, any population de-
clines of “front-line,” at-risk G. fulvus
may currently be masked by the in-
creased influx of winter migrants.
If disease spreads outside the In-
dian subcontinent, it will likely be
via G. fulvus and G. himalayensis
(Fig 1 ). As a conceptual tool, it is
useful to divide potential spread into
two phases: first, radiation from the
subcontinent through the centers of
distribution of Himalayan and Eur-
asian Griffons and, second, contin-
ued spread into European and Afri-
can Gyps. The distributions of
Eurasian and Himalayan Griffon vul-
tures (Ferguson-Lees & Christie 2000 )
and regional geography suggest four
routes of primary spread from the
subcontinent: ( A ) west through
southern Iran to the Zagros Moun-
tains ( G. fulvus ); ( B ) northwest
through Afghanistan and northern
Iran into the Caucasus (G. fulvus );
(C) north through the Pamir knot
and into the Tien-Shan of the
former Soviet Union (G. fulvus and
G. himalayensis ); and ( D) northeast
from the Himalayas onto the Tibetan
Plateau (G. himalayensis ) ( letters
match those on Fig. 2). A possible
fifth route (E ) could be across the
Straight of Hormuz from southern
Iran to the tip of the United Arab
Emirates (G. fulvus ).
The second stage of disease
spread, via G. fulvus, would likely
extend (F ) into the more fragmented
populations of the southern Alps and
Pyrenees in Europe and (G ) along
the mountains of the Middle East and
into Ethiopia and sub-Saharan Africa.
Passage into Africa could be from Jor-
dan and Israel down into Egypt and
then south into sub-Saharan Africa,
and/or across Saudi Arabia to Yemen
and across to Djibouti. Even where
there are obvious discrete gaps in
distribution between Gyps species,
we know some mixing between spe-
cies occurs because of the large dis-
tances individual birds travel. This
can be 1000 km or more (G. africa-
nus, G. coprotheres), and even resi-
dent breeding birds will forage 100
km from breeding sites ( Houston
1974, 1976; Ferguson Lees & Christie
2000). For example, a satellite-
tagged Eurasian griffon moved
1500 km from Israel to Yemen in
2002 (O. Bahat, personal communi-
cation, http://www.birds.org.il).
Current and Predicted Effects of
Vulture Declines
Gyps vultures are extremely effec-
tive and efficient scavengers. In the
Conservation Biology
Volume 17, No. 3, June 2003
Pain et al. Issues in International Conservation 667
Serengeti ecosystem in Tanzania, for
example, vultures are the major con-
sumers of dead ungulates, account-
ing for greater meat consumption
than all mammalian carnivores com-
bined (Houston 1979). A similar sit-
uation likely occurred in India prior
to the declines, particularly in the
many regions where Gyps vultures
were the primary scavengers.
The effective loss of Gyps vultures
from the Indian subcontinent will un-
doubtedly have important repercus-
sions, both for the environment and
for human health and well-being. For
example, an abundance of uneaten
carcasses (Prakash et al. 2003; V.P. et
al., unpublished observation) poses a
direct threat to public health because
the rotting flesh provides a breeding
ground for potentially pathogenic bac-
teria, posing the possibility of direct or
indirect infection. Uneaten carcasses
are also likely to provide sources of
disease, such as anthrax, for humans,
livestock, and wildlife. In removing
carcasses of large ungulates rapidly
and efficiently, vultures cleanse the en-
vironment. The acidic conditions in
the stomach of Gyps vultures kills
many pathogenic bacteria, such as an-
thrax, reducing the risk of disease
spread (Houston & Cooper 1975 ).
The ecological extinction of Gyps
vultures in India is also leading to
further changes in the species com-
plement of scavengers. The surfeit
of available food, for example, ap-
pears to be driving a rapid and
marked increase in the number of
small, predatory mammals, such as
feral dogs, and probably rats (Rattus
spp.). Such species have relatively
short lives and high reproductive
potential. At one carcass dump in
western Rajasthan, the numbers of
dogs increased from approximately 60
in 1992 to 1200 in 2000 (Prakash
et al. 2003; V.J. et al., unpublished
observation).
Because carcass dumps are often
close to human habitation, they cre-
ate a growing problem of dog at-
tacks on people, which can be fatal.
In addition, increasing populations
of feral rats and dogs pose a signifi-
cant risk of infectious disease to hu-
man beings, livestock, and wildlife.
As the populations of feral rats and
dogs increase, so too will the rates
of infectious disease transmission
within these populations and from
these species to others. Important
zoonotic diseases, such as rabies and
bubonic plague, which are endemic
within India and for which dogs and
rats, respectively, are the primary
reservoirs, are likely to increase as a
consequence of the vulture declines.
More humans die from rabies in Asia
than other regions, and the majority
of these deaths occur in India ( World
Health Organization 1998).
Wildlife and domestic livestock
may also be at increased risk from
dog- and rat-borne pathogens, in-
cluding canine distemper virus, ca-
nine parvovirus, and Leptospira spp.
bacteria. The increase in mammalian
scavengers at carcasses may have un-
known ecological consequences.
Most scavengers are also predatory,
and increases in their populations as
a result of the abundance of carrion
is likely to lead to higher predation
pressure on wildlife such as mam-
mals, ground-nesting birds, reptiles,
and amphibians.
Vultures are important not only
for environmental health but also for
Figure 2. Likely routes of spread from India of a Gyps-specific infectious disease. Shaded areas represent Gyps dis-
tributions. Likely routes of spread A–G are detailed in text.
Conservation Biology
Volume 17, No. 3, June 2003
668 Issues in International Conservation Pain et al.
their considerable cultural and reli-
gious significance in India and else-
where. For thousands of years and in
different parts of the world, humans
have laid out their dead for con-
sumption by scavengers (Schüz &
König 1983). Of these, the best
known and documented are the Par-
sees, 70% of whom live in Mumbai.
The Parsees believe that fire, earth,
and water are sacred and, as such,
must not be contaminated with hu-
man corpses. The Parsees therefore
ritualize the practice of putting out
the dead for scavengers by building
“towers of silence” to limit access to
corpses exclusively to airborne scav-
engers. In Mumbai the towers were
built 400 years ago and have become
an intrinsic part of the Parsees’ lives.
Until the population crash, vultures
visited the towers on a daily basis,
gathering on them at funeral time,
consuming almost the entire body
within half an hour. On average,
three bodies a day are placed in the
towers, but in the absence of vul-
tures only kites and crows visit, and
they are too small to have a signifi-
cant impact. The hygienic way of
disposing of their dead that the Par-
see practiced for generations has
gone, and they are faced with a di-
lemma. Some Parsees advocate a
more modern disposal method, such
as electrical cremation, whereas oth-
ers disagree and wish to adhere
strictly to their faith.
The economic impacts of the vul-
ture declines are manifold and include
the costs to villagers of disposing of
carcasses that would otherwise rot
and increase the risk of disease, the
costs associated with increased dog
bites and associated human disease,
and many others that are difficult to
quantify without detailed socio-
economic analyses. Collecting cattle
bones for the fertilizer industry is an
old trade among India’s poor, and
vultures effectively and rapidly
“cleaned” skeletons of all soft mate-
rial and facilitated the bone collec-
tor’s job. Today, carcasses are rot-
ting in areas with few scavengers,
and even where feral dog popula-
tions have increased massively, car-
casses are not cleaned thoroughly
because dogs only scavenge choice
tissues. This, and the attempted
burning of carcasses in some locali-
ties, removes a source of income for
the bone collectors.
Conclusions
Four of the eight species in the ge-
nus Gyps are now listed as globally
threatened; three of these are criti-
cal (BirdLife International 2000) be-
cause of the population crash across
the Indian subcontinent over the last
10–15 years. Massive declines in
avian scavengers and other large
birds have also occurred across
Southeast Asia, primarily during the
middle of the last century. Although
conclusive evidence is lacking, these
declines probably resulted from the
loss of wild ungulates and free-rang-
ing domestic cattle and water buf-
falo. Other factors such as persecu-
tion and pesticides may have played
a part in local demographic changes.
Today, relict populations of Gyps
vultures in Southeast Asia remain
only in and adjacent to Cambodia.
Gyps vultures were common or
abundant across much of the Indian
subcontinent until the late 1980s to
early 1990s, after which populations
of at least three species, G. benga-
lensis, G. indicus, and G. tenuiros-
tris, started to decline at an alarming
and unprecedented rate. These de-
clines have resulted in local extinc-
tions across much of India. The
causal factor(s) have not been identi-
fied, but it is extremely unlikely that
either food shortage or persecution
have played an important part. Al-
though the role of widespread con-
taminants has not been discounted,
current information suggests infec-
tious disease, possibly a genus-spe-
cific virus, as the most likely cause
of the declines. Should this prove to
be the case, there is real potential
for disease spread across the Middle
East and Central Asia, into Europe
and through Africa. Vulture declines
are already having a measurable eco-
logical impact in India and present
many risks to wildlife and human
health, social systems, and local
economies. Should Gyps vultures be
similarly affected in Africa, savanna
ecosystems and local people would
suffer similar effects.
That disease may be responsible
for such a dramatic and widespread
population crash is unusual because
it does not appear to be a major
cause of mortality in populations of
Gyps vultures elsewhere in the world
(Benson 2000). Diagnosis of disease
in wild bird populations is seldom at-
tempted, however, and the impor-
tance of disease as a population regu-
lator remains poorly understood and
probably greatly underestimated
(Daszak et al. 2000; Friend et al.
2001). If, as seems likely, infectious
disease is responsible for the declines,
it probably resulted from the intro-
duction of an alien disease, or per-
haps the introduction of a vector for a
disease from which the vultures were
previously ecologically isolated. It is
also possible that some environmen-
tal contaminant may have increased
their susceptibility to a disease to
which they were previously resistant.
Species that have evolved in the
absence of exposure to a particular
disease tend to be more susceptible
to its effects. A good example is the
endemic Hawaiian avifauna that, in
the absence of the mosquito vector,
had never been exposed to malarial
parasites, Plasmodium spp. although
they were probably present sporadi-
cally in Hawaii in the tissues of mi-
gratory birds. When the mosquito
vector, Culex quinquefasciatus, was
accidentally introduced in 1826, ma-
laria had a devastating effect on low-
elevation native forest birds, which
are particularly susceptible to this dis-
ease (Warner 1968; Atkinson et al.
1995 ). It is too early to speculate
about the possible origins of an infec-
tious disease affecting Gyps vultures,
but for a disease to have such a rapid
and devastating effect on a popula-
tion, it is likely to be something to
Conservation Biology
Volume 17, No. 3, June 2003
Pain et al. Issues in International Conservation 669
which the population was previ-
ously immunologically naive.
Research and Monitoring Needs
Identifying the mortality factor(s) re-
sponsible for the vulture declines is an
obvious priority. Until this has been
done, it will be extremely difficult to
identify action needed to improve the
situation where declines have oc-
curred or arrest the spread of the
problem. Although current informa-
tion suggests that investigations
should focus on an infectious disease
as the most likely cause, it is important
that other potential causes, particu-
larly the role of contaminants, are not
ignored. Even if infectious disease has
played a part in the declines, there
may be other underlying factors.
On the basis of current evidence, it
is realistic to assume that the mortal-
ity factor will continue to spread and
could rapidly move beyond the In-
dian subcontinent. G. fulvus is the
species most likely to facilitate the
spread of disease from India and Paki-
stan across the Middle East and Cen-
tral Asia and into Europe and Africa.
Monitoring of the number and health
status of Gyps species at colonies
across their range states should be
initiated rapidly to identify the routes
and rate of spread of the problem.
Satellite tracking of G. fulvus in India
and across the Middle East is under-
way to help elucidate the most likely
routes of spread. Although monitor-
ing of Gyps species is essential, other
avian scavengers should not be ig-
nored. Other species do not appear
to have suffered the fate of Gyps vul-
tures, but monitoring is poor or non-
existent, and there is not yet conclu-
sive evidence that Gyps species alone
are affected.
There is an urgent need to con-
serve the relict Gyps populations in
Cambodia and adjacent parts of Laos
and Vietnam. Should the cause of de-
clines prove to be infectious disease,
these populations will assume in-
creasing importance because they are
now relatively isolated, with a low
risk of exposure to the agent killing
birds in India. It is therefore impor-
tant to reverse the population decline
there through effective conservation
management in northeastern Cambo-
dia. Efforts should also be made to
use the small numbers of G. benga-
lensis in captivity in Western Europe
and elsewhere to initiate a captive
breeding program to guard against
the extinction of this species. We
know of no G. indicus or G. tenuiros-
tris in captivity.
Declines of the scale and rapidity
seen in Gyps vultures are unprece-
dented for a large bird of prey. Con-
servation of Gyps species requires a
concerted international effort, in-
volving a wide range of disciplines,
including biologists, wildlife pathol-
ogists, epidemiologists, and captive
breeding specialists. These declines
do not simply represent the poten-
tial extinction of a species or, even-
tually, a genus, serious though ex-
tinction would be. Vultures are
keystone species, and their disap-
pearance is having and will have ma-
jor impacts on both the ecosystems
they inhabit and the humans associ-
ated with them.
It is rare that nothing can be done
to stem or manage a decline when
the causal agent has been identified.
Although unlikely, it is possible that
no action can be taken to stem the
Gyps declines. Should this be the
case, at a minimum, actions should
be identified that will minimize the
consequences for wildlife and human
health of loss of Gyps vultures in Afri-
can ecosystems and elsewhere.
Acknowledgments
We thank M. Virani of the Peregrine
Fund for useful discussions, D. Gib-
bons for comments on the manu-
script, and J. Ginsberg for suggesting
this piece and for his helpful com-
ments. Much of the research on vul-
tures in India was funded by the Dar-
win Initiative for the Survival of
Species (United Kingdom) and the
U.S. Fish and Wildlife Service.
D. J. Pain
Royal Society for the Protection of Birds, The
Lodge, Sandy, Bedfordshire SG19 2DL, United
Kingdom, email debbie.pain@rspb.org.uk
A. A. Cunningham
Institute of Zoology, Zoological Society of Lon-
don, Regent’s Park, London NW1 4RY, United
Kingdom
P. F. Donald
Royal Society for the Protection of Birds, The
Lodge, Sandy, Bedfordshire SG19 2DL, United
Kingdom
J. W. Duckworth
Wildlife Conservation Society, 2300 Southern
Boulevard, Bronx, NY 10460–1099, U.S.A., and
East Redham Farm, Pilning, Bristol BS35 4JG,
United Kingdom
D. C. Houston
Graham Kerr Building, Glasgow University, Glas-
gow G12 8QQ, United Kingdom
T. Katzner
Department of Biology, Arizona State University,
P.O. Box 871501, Tempe, AZ 85287–1501, U.S.A.,
and Wildlife Conservation Society, Central Asia
Program, 2300 Southern Boulevard, Bronx, NY
10460, U.S.A.
J. Parry-Jones
The National Birds of Prey Centre, Newent,
Gloucestershire, GL18 1JJ, United Kingdom
C. Poole
Wildlife Conservation Society, Cambodia Pro-
gramme, P.O. Box 1620, Phnom Penh, Cambodia
V. Prakash
Bombay Natural History Society (BNHS ), Horn-
bill House, Shaheed Bhagat Singh Road, Mumbai,
400023, India
P. Round
Department of Biology, Faculty of Science, Mahi-
dol University, Rama 6 Road, Bangkok 10400,
Thailand
R. Timmins
2313 Willard Avenue, Madison, WI 53704, U.S.A.
Conservation Biology
Volume 17, No. 3, June 2003
670 Issues in International Conservation Pain et al.
Literature Cited
Atkinson, C. T., K. L. Woods, R. J. Dusek, L. S.
Sileo, and W. M. Iko. 1995. Wildlife disease
and conservation in Hawaii: pathogenicity
of avian malaria (Plasmodium relictum ) in
experimentally infected Iiwi (Vestiaria
coccinea). Parasitology 111:S59–S69.
Benson, P. C. 2000. Causes of Cape Vulture
Gyps coprotheres mortality at the Krans-
berg colony: a 17-year update. Pages 77–
86 in R. D. Chancellor and B.-U. Meyburg,
editors. Raptors at risk: proceedings of the
5th world conference on birds of prey and
owls. Hancock House Publishers, Wash-
ington, D.C., and World Working Group
on Birds of Prey and Owls, Berlin.
BirdLife International. 2000. Threatened birds
of the world. Lynx Edicions, Barcelona, and
BirdLife International, Cambridge, United
Kingdom.
BirdLife International. 2001. Threatened birds
of Asia: the BirdLife International red data
book. BirdLife International, Cambridge,
United Kingdom.
Cambodian Wetland Team. 2001. Final report
on participatory rural appraisal in Boung
Rei village, Sambo District, Kratie Prov-
ince, Mekong River. Royal Government of
Cambodia, Inventory and Management of
Cambodian Wetlands Project (MRC–Danida),
Phnom Penh.
Cheke, A. 1972. Where no vultures fly. World
of Birds 2(1):15–22.
Cunningham, A. A., V. Prakash, G. R. Ghalsasi,
and D. Pain. 2001. Investigating the cause
of catastrophic declines in Asian Griffon
Vultures (Gyps indicus and G. bengalensis ).
Pages 10–11 in T. Katzner, and J. Parry-Jones,
editors. Reports from the workshop on In-
dian Gyps vultures. Proceedings of theth
Eurasian congress on raptors. Estación Bi-
ológica Donaña, Raptor Research Founda-
tion, Seville.
Cunningham, A. A., V. Prakash, D. J. Pain,
G. R. Ghalsasi, G. A. H. Wells, G. N.
Kolte, P. Nighot, M. S. Goudar, S. Kshirsa-
gar, and A. Rahami. In press. Indian vul-
tures: victims of an infectious disease epi-
demic? Animal Conservation.
Daszak, P., A. A. Cunningham, and A. D.
Hyatt. 2000. Review: emerging infectious
diseases of wildlife: threats to biodiversity
and human health. Science 287:443–449.
Deignan, H. G. 1945. The birds of northern
Thailand. Bulletin 186. U.S. National Mu-
seum, Washington, D.C.
Deignan, H. G. 1963. Checklist of the birds of
Thailand. Bulletin 226. U.S. National Mu-
seum, Washington, D.C.
del Hoyo, J., A. Elliott, and J. Sargatal, editors.
1994. Handbook of birds of the world. 2.
New World vultures to Guineafowl. Lynx
Edicions, Barcelona.
Delacour, J., and P. Jabouille. 1931. Les
oiseaux de l’Indochine française, 1–4. Ex-
position Coloniale Internationale, Paris.
Duckworth, J. W., R. E. Salter, and K. Khoun-
boline, compilers. 1999. Wildlife in Lao
PDR: 1999 status report. The World Con-
servation Union, Wildlife Conservation
Society, Centre for Protected Areas and
Watershed Management, Gland, Switzerland.
Duckworth, J. W., P. Davidson, T. D. Evans,
P. D. Round, and R. J. Timmins. 2002. Bird
records from North Laos, principally
Xiangkhouang Province and the upper
Lao Mekong, in 1998–2000. Forktail 18:
11–44.
Ferguson-Lees, J., and D. A. Christie. 2000.
Raptors of the world: identification guides.
Christopher Helm, London.
Friend, M., R. G. McLean, and F. J. Dein. 2001.
Disease emergence in birds: challenges
for the twenty-first century. The Auk 118:
290–303.
Galushin, V. M. 1971. A huge urban popula-
tion of birds of prey in Delhi, India. Ibis
113:522.
Gilbert, M., M. Z. Virani, R. T. Watson, J. L.
Oaks, P. C. Benson, A. A. Khan, S. Ahmed,
J. Chaudhry, M. Arshad, S. Mahmood, and
Q. A. Shah. 2002. Breeding and mortality of
Oriental White-backed Vulture Gyps ben-
galensis in Punjab Province, Pakistan. Bird
Conservation International. 12:311–326.
Goes, F. 1999. Notes on selected bird species
in Cambodia. Forktail 15:25–27.
Griesinger, J. 1996. Autumn migration of grif-
fon vultures (Gyps f. fulvus ) in Spain.
Pages 401–410 in J. Muntaner and J. Mayol,
editors. Biología conservación de las ra-
paces Mediterráneas, 1994. Monograph.
Sociedad Española de Ornitologia/BirdLife
International, Madrid.
Grubh, R. B., G. Narayam, and S. M. Sathee-
san. 1990. Conservation of vultures in (de-
veloping) India. Pages 360–363 in J. C.
Daniel and J. S. Serrao, editors. Conserva-
tion in developing countries. Bombay Nat-
ural History Society/Oxford University
Press, Bombay.
Guangmei, Z., and W. Qishan. 1998. China
red data book of endangered animals: Aves.
Science Press, Beijing.
Hilton-Taylor, C. 2000. 2000 IUCN red list of
threatened species. World Conservation
Union (IUCN ), Gland, Switzerland.
Houston, D. C. 1974. Food searching in grif-
fon vultures. East African Wildlife Journal
12:63–77.
Houston, D. C. 1976. Breeding of the white-
backed and Ruppell’s griffon vultures. Ibis
118:14–39.
Houston, D. C. 1979. The adaptation of scav-
engers. Pages 263–286 in A. R. E. Sinclair
and N. Griffiths, editors. Serengeti, dynam-
ics of an ecosystem. University of Chicago
Press, Chicago.
Houston, D. C. 1983. The adaptive radiation
of the griffon vultures. Pages 135–152 in
S. R. Wilbur and J. A. Jackson, editors. Vul-
ture biology and management. University
of California Press, Berkeley.
Houston, D. C. 1985. Indian white-backed
vulture (G. bengalensis ). Pages 465–466
in I. Newton, R.D. Chancellor, editors.
Conservation studies on raptors. Techni-
cal publication 5. International Council
for Bird Preservation Cambridge, United
Kingdom.
Houston, D. C., and J. E. Cooper. 1975. The
digestive tract of the whitebacked griffon
vulture and its role in disease transmission
among wild ungultates. Journal of Wildlife
Diseases 11:306–313.
Husein, K. Z., and S. U. Sarkar. 1971. Notes
on a collection of birds from Pabnar
(Bangladesh). Journal of the Asiatic Soci-
ety of Bangladesh. 16:259–288.
Inskipp, C., and T. P. Inskipp. 1991. A guide
to the birds of Nepal. Smithsonian Institu-
tion Press, Washington, D.C.
Inskipp, C., and T. P. Inskipp. 1993. Birds re-
corded during a visit to Bhutan in spring
1993. Forktail 9:121–142.
Le Xuan Canh, Pham Trong Anh, J. W. Duck-
worth, Vu Ngoc Thanh, and Lic Vuthy.
1997. A survey of large mammals in Dak
Lak Province, Vietnam. WWF/IUCN, Hanoi.
Lekagul, B., and P. D. Round. 1991. A guide to
the birds of Thailand. Saha Karn Bhaet,
Bangkok.
Mendelssohn, H., and Y. Leshem. 1983. Ob-
servations on reproduction and growth of
Old World vultures. Pages 214–244 in
S. R. Wilber and J. A. Jackson, editors. Vul-
ture biology and management. University
of California Press, Berkeley.
Mundy, P., D. Butchart, J. Ledger, and S. Piper.
1992. The vultures of Africa. Academic
Press, London.
Newton, I. 1979. Population ecology of rap-
tors. T. and A. D. Poyser, editors. Berkhemp-
sted, United Kingdom.
Newton, I., J. Bogan, E. Meek, and B. Little.
1982. Organochlorine compounds and
shell-thinning in British merlins (Falco
columbarius). Ibis 124:238–335.
Newton, I., J. A. Bogan, and P. Rothery. 1986.
Trends and effects of organochlorine com-
pounds in Sparrowhawk eggs. Journal of
Applied Ecology 23:461–478.
Oaks, L., and B. A. Rideout, M. Gilbert, R. Wat-
son, M. Virani, and A. Ahmed Khan. 2001.
Summary of diagnostic investigation into
vulture mortality: Punjab Province, Paki-
stan, 2000–2001. Reports from the work-
shop on Indian Gyps vultures. Pages 12–13
in T. Katzner, and J. Parry-Jones, editors.
Proceedings of the 4th Eurasian congress
on raptors. Estación Biológica Donaña,
Raptor Research Foundation, Seville.
Pain, D. J., V. Prakash, A. A. Cunningham, and
G. R. Ghalsasi. 2002. Vulture declines in
India: patterns, causes and spread. Pages
4–7 in T. Katzner and J. Parry-Jones, edi-
tors. Conservation of Gyps Vulture in Asia.
3rd North American Ornithological Con-
gress, September 24–28, 2002. New Or-
leans, LA, USA.
Conservation Biology
Volume 17, No. 3, June 2003
Pain et al. Issues in International Conservation 671
Prakash, V. 1989. The general ecology of
raptors (Families: Accipitridae, Strigidae,
Class: Aves) in Keoladeo National Park,
Bharatpur. Ph.D. thesis. Bombay Natural
History Society, Bombay University,
Mumbai.
Prakash, V. 1999. Status of vultures in Ke-
oladeo National Park, Bharatpur, Rajast-
han, with special reference to population
crash in Gyps species. Journal of the Bom-
bay Natural History Society 96:365–378.
Prakash, V., D. J. Pain, A. A. Cunningham,
P. F. Donald, N. Prakash, A. Verma, R.
Gargi, S. Sivakumar, and A. R. Rahmani.
2003. Catastrophic collapse of Indian
white-backed Gyps bengalensis and long-
billed Gyps indicus vulture populations.
Biological Conservation 109:381–390
Rahmani, A. 1998. A possible decline of vul-
tures in India. Oriental Bird Club Bulletin
28:40–41.
Rand, A. L. and R. L. Fleming. 1957. Birds of
Nepal. Fieldiana Zoology 41:1–218.
Rasmussen, P. C., and S. J. Parry. 2000. On the
specific distinctness of the Himalayan Long-
billed Vulture Gyps [indicus] tenuirostris.
Page 16. 118th stated meeting of the Ameri-
can Ornithologists’ Union (AOU ). AOU,
Memorial University of Newfoundland, St.
John’s, Newfoundland.
Ratcliffe, D. A. 1967a. Decrease in eggshell
weight in certain birds of prey. Nature
215:208–210.
Ratcliffe, D. A. 1967b. The peregrine situation
in Great Britain: 1965–1966. Bird Study
14:238–246.
Roberts, T. J. 1991–1992. The birds of Paki-
stan. Oxford University Press, Karachi.
Robson, C. 2000. A guide to the birds of South-
east Asia. Princetown University Press, Prin-
ceton, New Jersey.
Robson, C. R., H. Buck, D. S. Farrow, T.
Fisher, and B. F. King. 1998. A birdwatch-
ing visit to the Chin Hills, West Burma
(Myanmar ), with notes from nearby areas.
Forktail 13:109–120.
Round, P. D. 1988. Resident forest birds in
Thailand. Monograph 2. International Coun-
cil for Bird Preservation, Cambridge, United
Kingdom.
Round, P. D. 2000. Field check-list of Thai
birds. Bird Conservation Society of Thai-
land, Bangkok.
Sarrazin, F., C. Bagnolini, J.-L. Pinna, E. Danchin,
and J. Clobert. 1994. High survival estimates
of griffon vultures (Gyps fulvus fulvus ) in a
reintroduced population. The Auk 111:
853–862.
Schüz, E., and C. König. 1983. Old World
vultures and man. Pages 461–469 in S. R.
Wilbur and J. A. Jackson, editors. Vulture
biology and management. University of
California Press, Berkely.
Scully, J. 1879. A contribution to the ornithol-
ogy of Nepal. Stray Feathers 8:204–368.
Simmons, R. 1986. Delayed breeding and the
non-adaptive significance of delayed matu-
rity in vultures: a fruit fly perspective. Vul-
ture News 15:13–18.
Smythies, B. E. 1953. The birds of Burma.
2nd edition. Oliver and Boyd, Edinburgh,
United Kingdom.
Srikosamatara, S., and V. Suteethorn. 1995.
Populations of Gaur and Banteng and their
management in Thailand. Natural History
Bulletin of the Siam Society 43:55–83.
Thewlis, R. M., R. J. Timmins, T. D. Evans,
and J. W. Duckworth. 1998. The conserva-
tion status of birds in Laos: a review of key
species. Bird Conseration International 8
(supplement):1–159.
Timmins, R. J., and Men Soriyun 1998. A wild-
life survey of the Tonle San and Tonle Sre-
pok river basins in north-eastern Cambo-
dia. Fauna and Flora International and
Wildlife Protection Office, Hanoi.
Timmins, R. J., and Ou Ratanak 2001. The im-
portance of Phnom Prich Wildlife Sanctu-
ary and adjacent areas for the conserva-
tion of tigers and other key species. World
Wildlife Foundation, Indochina Programme,
Hanoi.
Tso-hsin, C. 1987. A synopsis of the avifauna
of China. Science Press, Beijing.
Virani, M., M. Gilbert, R. Watson, L. Oaks, and
P. Benson, A. A. Kham, and H.-S. Baral.
2001. Asian vulture crisis project: field re-
sults from Pakistan and Nepal for the
2000–2001 field season. Reports from the
workshop on Indian Gyps vultures. Pages
7–9 in T. Katzner and J. Parry-Jones, editors.
Proceedings of the 4th Eurasian congress
on raptors. Estación Biológica Donaña, Rap-
tor Research Foundation, Seville.
Warner, R. E. 1968. The role of introduced
diseases in the extinction of the endemic
Hawaiian avifauna. Condor 70:101–120.
Wells, D. R. 1984. Bird report: 1978 & 1979.
Malayan Nature Journal 38:113–150.
Wells, D. R. 1999. The birds of the Thai-Malay
Peninsula. 1. Non-passerines. Academic Press,
London.
Wildash, P. 1968. Birds of South Vietnam.
Tuttle & Company, Rutland, Vermont.
World Health Organization (WHO ). 1998.
World survey for rabies no. 34 for the year
1998. WHO, Geneva.
